Mountain caves of the central region of Veracruz: A vertebrate biodiversity reservoir in a Neotropical hotspot.

The mountain region of central Veracruz, Mexico hosts a large system of karst and volcanic caves that are unexplored. In particular, the vertebrates that inhabit these subterranean ecosystems are unknown. This study evaluated the diversity of mammals, birds, reptiles, amphibians, and fish in three environments (euphotic, disphotic, and aphotic) of 16 caves of different geological origin (12 karst caves and 4 volcanic caves) distributed along an altitudinal gradient (300-2400 m a.s.l.). We found a richness of 242 vertebrate species (184 birds, 30 mammals, 15 reptiles, 12 amphibians, and 1 fish) and an abundance of a total of 11,323 individuals (4,969 mammals, 6,483 birds, 36 reptiles, 27 amphibians, and 5 fish). The richness of all vertebrate classes was higher in karst than in volcanic caves. Vertebrate diversity was also higher at mid-altitudes between 600-899 m a.s.l. Diversity varied between environments, where bird and reptile richness was higher in the euphotic environment, while mammal and amphibian diversity was higher in the aphotic environment. The similarity in the composition of vertebrate species does not depend on the distance between karstic and volcanic caves. Volcanic and karst caves shared on average up to 70% and 55% of vertebrate species, which indicates that only 30% and 45% of species, respectively, is different in each cave type. Given the vulnerability and fragility of these subterranean ecosystems, as well as the important diversity that they contain, we recommend including the caves of the central region of Veracruz in the conservation agenda of local governments and communities. Community-based conservation can help ensure the presence of vertebrate species in the caves of this region.

A new pseudosuchian from the Favret Formation of Nevada reveals that archosauriforms occupied coastal regions globally during the Middle Triassic.

Recent studies suggest that both stem- and crown-group Archosauria encompassed high ecological diversity during their initial Triassic radiation. We describe a new pseudosuchian archosaur, Benggwigwishingasuchus eremicarminis gen. et sp. nov., from the Anisian (Middle Triassic) Fossil Hill Member of the Favret Formation (Nevada, USA), a pelagic setting in the eastern Panthalassan Ocean characterized by the presence of abundant ammonoids and large-bodied ichthyosaurs. Coupled with archosauriforms from the eastern and western Tethys Ocean, Benggwigwishingasuchus reveals that pseudosuchians were also components of Panthalassan ocean coastal settings, establishing that the group occupied these habitats globally during the Middle Triassic. However, Benggwigwishingasuchus, Qianosuchus, and Ticinosuchus (two other pseudosuchians known from marine sediments) are not recovered in a monophyletic group, demonstrating that a nearshore marine lifestyle occurred widely across Archosauriformes during this time. Benggwigwishingasuchus is recovered as part of an expanded Poposauroidea, including several taxa (e.g. Mandasuchus, Mambawakalae) from the Middle Triassic Manda Beds of Tanzania among its basally branching members. This implies a greater undiscovered diversity of poposauroids during the Early Triassic, and supports that the group, and pseudosuchians more broadly, diversified rapidly following the End-Permian mass extinction.

A phylogeny-informed characterisation of global tetrapod traits addresses data gaps and biases.

Tetrapods (amphibians, reptiles, birds, and mammals) are model systems for global biodiversity science, but continuing data gaps, limited data standardisation, and ongoing flux in taxonomic nomenclature constrain integrative research on this group and potentially cause biased inference. We combined and harmonised taxonomic, spatial, phylogenetic, and attribute data with phylogeny-based multiple imputation to provide a comprehensive data resource (TetrapodTraits 1.0.0) that includes values, predictions, and sources for body size, activity time, micro- and macrohabitat, ecosystem, threat status, biogeography, insularity, environmental preferences, and human influence, for all 33,281 tetrapod species covered in recent fully sampled phylogenies. We assess gaps and biases across taxa and space, finding that shared data missing in attribute values increased with taxon-level completeness and richness across clades. Prediction of missing attribute values using multiple imputation revealed substantial changes in estimated macroecological patterns. These results highlight biases incurred by nonrandom missingness and strategies to best address them. While there is an obvious need for further data collection and updates, our phylogeny-informed database of tetrapod traits can support a more comprehensive representation of tetrapod species and their attributes in ecology, evolution, and conservation research.

Macroecological correlates of Darwinian shortfalls across terrestrial vertebrates.

Most described species have not been explicitly included in phylogenetic trees-a problem named the Darwinian shortfall-owing to a lack of molecular and/or morphological data, thus hampering the explicit incorporation of evolution into large-scale biodiversity analyses. We investigate potential drivers of the Darwinian shortfall in tetrapods, a group in which at least one-third of described species still lack phylogenetic data, thus necessitating the imputation of their evolutionary relationships in fully sampled phylogenies. We show that the number of preserved specimens in scientific collections is the main driver of phylogenetic knowledge accumulation, highlighting the major role of biological collections in unveiling novel biodiversity data and the importance of continued sampling efforts to reduce knowledge gaps. Additionally, large-bodied and wide-ranged species, as well as terrestrial and aquatic amphibians and reptiles, are phylogenetically better known. Future efforts should prioritize phylogenetic research on organisms that are narrow-ranged, small-bodied and underrepresented in scientific collections, such as fossorial species. Addressing the Darwinian shortfall will be imperative for advancing our understanding of evolutionary drivers shaping biodiversity patterns and implementing comprehensive conservation strategies.

Differential Conservation and Loss of Chicken Repeat 1 (CR1) Retrotransposons in Squamates Reveal Lineage-Specific Genome Dynamics Across Reptiles.

Transposable elements (TEs) are repetitive DNA sequences which create mutations and generate genetic diversity across the tree of life. In amniote vertebrates, TEs have been mainly studied in mammals and birds, whose genomes generally display low TE diversity. Squamates (Order Squamata; including ∼11,000 extant species of lizards and snakes) show as much variation in TE abundance and activity as they do in species and phenotypes. Despite this high TE activity, squamate genomes are remarkably uniform in size. We hypothesize that novel, lineage-specific genome dynamics have evolved over the course of squamate evolution. To understand the interplay between TEs and host genomes, we analyzed the evolutionary history of the chicken repeat 1 (CR1) retrotransposon, a TE family found in most tetrapod genomes which is the dominant TE in most reptiles. We compared 113 squamate genomes to the genomes of turtles, crocodilians, and birds and used ancestral state reconstruction to identify shifts in the rate of CR1 copy number evolution across reptiles. We analyzed the repeat landscapes of CR1 in squamate genomes and determined that shifts in the rate of CR1 copy number evolution are associated with lineage-specific variation in CR1 activity. We then used phylogenetic reconstruction of CR1 subfamilies across amniotes to reveal both recent and ancient CR1 subclades across the squamate tree of life. The patterns of CR1 evolution in squamates contrast other amniotes, suggesting key differences in how TEs interact with different host genomes and at different points across evolutionary history.

A new small-sized predatory pseudosuchian archosaur from the Middle-Late Triassic of Southern Brazil.

Before the rise of dinosaurs and pterosaurs, pseudosuchians-reptiles from the crocodilian lineage-dominated the Triassic land ecosystems. This lineage diversified into several less inclusive clades, resulting in a wide ecomorphological diversity during the Middle and Late Triassic. Some giant pseudosuchians occupied the top of the trophic webs, while others developed extensive bony armor as a defense mechanism, which later evolved as a convergence in the avemetatarsalian lineage. On the other hand, there were groups like the Gracilisuchidae, which was composed of carnivorous forms with lightweight build and less than 1 m in length. The fossil record of gracilisuchids is geographically restricted to China and Argentina, with one ambiguous record from Brazil. In the present study, the first unambiguous gracilisuchid from Brazil is described. Parvosuchus aurelioi gen. et sp. nov. comes from the Dinodontosaurus Assemblage Zone of the Santa Maria Formation, which is associated with the Ladinian-Carnian boundary. Composed of a complete cranium, vertebrae, pelvic girdle and hindlimbs, the new species nests with Gracilisuchus stipanicicorum and Maehary bonapartei in a phylogenetic analysis. Its discovery fills a taxonomic gap in Brazilian pseudosuchian fauna and reveals the smallest known member of this clade from the Dinodontosaurus Assemblage Zone, highlighting the diversity of pseudosuchians during the moment that preceded the dawn of dinosaurs.

Oldest southern sauropterygian reveals early marine reptile globalization.

Sauropterygians were the stratigraphically longest-ranging clade of Mesozoic marine reptiles with a global fossil record spanning ∼180 million years1. However, their early evolution has only been known from what is now the Northern Hemisphere, extending across the northern and trans-equatorial western margins of the Tethys paleo-ocean1 after the late-Early Triassic (late Olenekian, ∼248.8 million years [Ma] ago2), and via possible trans-Arctic migration1 to the Eastern Panthalassa super-ocean prior to the earliest Middle Triassic (Olenekian-earliest Anisian3,4, ∼247 Ma). Here, we describe the geologically oldest sea-going reptile from the Southern Hemisphere - a nothosaur (basal sauropterygian5) from the Middle Triassic (Anisian, after ∼246 Ma6) of New Zealand. Time-scaled ancestral range estimations thus reveal an unexpected circum-Gondwanan high-paleolatitude (>60° S7) dispersal from a northern Tethyan origination center. This coincides with the adaptive diversification of sauropterygians after the end-Permian mass extinction8 and suggests that rapid globalization accompanied their initial radiation in the earliest Mesozoic.

Tetrapod biodiversity in sambaquis from southern Brazil.

Fishermen-hunter-gatherers of sambaquis (Brazilian shell mounds) had an intimate affinity with marine-coastal environments, where they exploited a great variety of fish and mollusks that comprise the best documented fauna from sambaquis. However, other groups of animals as mammals, birds, reptiles, and amphibians are also present in these sites, but are relatively less studied. This paper is the first one focused exclusively on the Tetrapoda biodiversity of sambaquis and aimed to identify tetrapods of ten sites from southern Brazil. We present a faunal inventory and data regarding animal capture and environmental exploitation. We identified the specimens anatomically and taxonomically, analyzed them concerning fragmentation, and quantified the data for the number of identified specimens (NISP) and minimum number of individuals (MNI). Despite the high degree of fragmentation of remains, we identified 46 taxa. As expected, most were from marine animals: cetaceans (total NISP = 2,568 and MNI = 27), otariids (total NISP = 248 and MNI = 32), and seabirds (total NISP = 65 and MNI = 23), indicating great relevance of marine tetrapod fauna as a resource for sambaqui builders (79.39% of NISP). We thus document the close bond between fishermen-hunter-gatherers of sambaquis and the marine tetrapods in southern Brazil.

Cranial anatomy of Emeroleter levis and the phylogeny of Nycteroleteridae.

Among the diverse basal reptile clade Parareptilia, the nycteroleters are among the most poorly understood. The interrelationships of nycteroleters are contentious, being recovered as both monophyletic and paraphyletic in different analyses, yet their anatomy has received little attention. We utilized x-ray computed tomography to investigate the skull of the nycteroleterid Emeroleter levis, revealing aspects of both the external and internal cranial anatomy that were previously unknown or undescribed, especially relating to the palate, braincase, and mandible. Our results reveal a greater diversity in nycteroleter cranial anatomy than was previously recognized, including variation in the contribution of the palatal elements to the orbitonasal ridge among nycteroleters. Of particular note are the unique dentition patterns in Emeroleter, including the presence of dentition on the ectopterygoid, an element which is typically edentulous in most parareptiles. We then incorporate the novel information gained from the computed tomography analysis into an updated phylogenetic analysis of parareptiles, producing a fully resolved Nycteroleteridae and further supporting previous suggestions that the genus 'Bashkyroleter' is paraphyletic.

Threats to reptiles at global and regional scales.

Reptiles are an important, yet often understudied, taxon in nature conservation. They play a significant role in ecosystems1 and can serve as indicators of environmental health, often responding more rapidly to human pressures than other vertebrate groups.2 At least 21% of reptiles are currently assessed as threatened with extinction by the IUCN.3 However, due to the lack of comprehensive global assessments until recently, they have been omitted from spatial studies addressing conservation or spatial prioritization (e.g., Rosauer et al.,4,5,6,7,8 Fritz and Rahbek,4,5,6,7,8 Farooq et al.,4,5,6,7,8 Meyer et al., 4,5,6,7,8 and Farooq et al.4,5,6,7,8). One important knowledge gap in conservation is the lack of spatially explicit information on the main threats to biodiversity,9 which significantly hampers our ability to respond effectively to the current biodiversity crisis.10,11 In this study, we calculate the probability of a reptile species in a specific location being affected by one of seven biodiversity threats-agriculture, climate change, hunting, invasive species, logging, pollution, and urbanization. We conducted the analysis at a global scale, using a 50 km × 50 km grid, and evaluated the impact of these threats by studying their relationship with the risk of extinction. We find that climate change, logging, pollution, and invasive species are most linked to extinction risk. However, we also show that there is considerable geographical variation in these results. Our study highlights the importance of going beyond measuring the intensity of threats to measuring the impact of these separately for various biogeographical regions of the world, with different historical contingencies, as opposed to a single global analysis treating all regions the same.

Protected areas slow declines unevenly across the tetrapod tree of life.

Protected areas (PAs) are the primary strategy for slowing terrestrial biodiversity loss. Although expansion of PA coverage is prioritized under the Convention on Biological Diversity, it remains unknown whether PAs mitigate declines across the tetrapod tree of life and to what extent land cover and climate change modify PA effectiveness1,2. Here we analysed rates of change in abundance of 2,239 terrestrial vertebrate populations across the globe. On average, vertebrate populations declined five times more slowly within PAs (-0.4% per year) than at similar sites lacking protection (-1.8% per year). The mitigating effects of PAs varied both within and across vertebrate classes, with amphibians and birds experiencing the greatest benefits. The benefits of PAs were lower for amphibians in areas with converted land cover and lower for reptiles in areas with rapid climate warming. By contrast, the mitigating impacts of PAs were consistently augmented by effective national governance. This study provides evidence for the effectiveness of PAs as a strategy for slowing tetrapod declines. However, optimizing the growing PA network requires targeted protection of sensitive clades and mitigation of threats beyond PA boundaries. Provided the conditions of targeted protection, adequate governance and well-managed landscapes are met, PAs can serve a critical role in safeguarding tetrapod biodiversity.

High phenotypic plasticity at the dawn of the eosauropterygian radiation.

The initial radiation of Eosauropterygia during the Triassic biotic recovery represents a key event in the dominance of reptiles secondarily adapted to marine environments. Recent studies on Mesozoic marine reptile disparity highlighted that eosauropterygians had their greatest morphological diversity during the Middle Triassic, with the co-occurrence of Pachypleurosauroidea, Nothosauroidea and Pistosauroidea, mostly along the margins of the Tethys Ocean. However, these previous studies quantitatively analysed the disparity of Eosauropterygia as a whole without focussing on Triassic taxa, thus limiting our understanding of their diversification and morphospace occupation during the Middle Triassic. Our multivariate morphometric analyses highlight a clearly distinct colonization of the ecomorphospace by the three clades, with no evidence of whole-body convergent evolution with the exception of the peculiar pistosauroid Wangosaurus brevirostris, which appears phenotypically much more similar to nothosauroids. This global pattern is mostly driven by craniodental differences and inferred feeding specializations. We also reveal noticeable regional differences among nothosauroids and pachypleurosauroids of which the latter likely experienced a remarkable diversification in the eastern Tethys during the Pelsonian. Our results demonstrate that the high phenotypic plasticity characterizing the evolution of the pelagic plesiosaurians was already present in their Triassic ancestors, casting eosauropterygians as particularly adaptable animals.

New reptile shows dinosaurs and pterosaurs evolved among diverse precursors.

Dinosaurs and pterosaurs have remarkable diversity and disparity through most of the Mesozoic Era1-3. Soon after their origins, these reptiles diversified into a number of long-lived lineages, evolved unprecedented ecologies (for example, flying, large herbivorous forms) and spread across Pangaea4,5. Recent discoveries of dinosaur and pterosaur precursors6-10 demonstrated that these animals were also speciose and widespread, but those precursors have few if any well-preserved skulls, hands and associated skeletons11,12. Here we present a well-preserved partial skeleton (Upper Triassic, Brazil) of the new lagerpetid Venetoraptor gassenae gen. et sp. nov. that offers a more comprehensive look into the skull and ecology of one of these precursors. Its skull has a sharp, raptorial-like beak, preceding that of dinosaurs by around 80 million years, and a large hand with long, trenchant claws that firmly establishes the loss of obligatory quadrupedalism in these precursor lineages. Combining anatomical information of the new species with other dinosaur and pterosaur precursors shows that morphological disparity of precursors resembles that of Triassic pterosaurs and exceeds that of Triassic dinosaurs. Thus, the 'success' of pterosaurs and dinosaurs was a result of differential survival among a broader pool of ecomorphological variation. Our results show that the morphological diversity of ornithodirans started to flourish among early-diverging lineages and not only after the origins of dinosaurs and pterosaurs.

Description and phylogenetic relationships of a new species of Torvoneustes (Crocodylomorpha, Thalattosuchia) from the Kimmeridgian of Switzerland.

Metriorhynchids are marine crocodylomorphs found across Jurassic and Lower Cretaceous deposits of Europe and Central and South America. Despite being one of the oldest fossil families named in paleontology, the phylogenetic relationships within Metriorhynchidae have been subject to many revisions over the past 15 years. Herein, we describe a new metriorhynchid from the Kimmeridgian of Porrentruy, Switzerland. The material consists of a relatively complete, disarticulated skeleton preserving pieces of the skull, including the frontal, prefrontals, right postorbital, nasals, maxillae, right premaxillae and nearly the entire mandible, and many remains of the axial and appendicular skeleton such as cervical, dorsal, and caudal vertebrae, ribs, the left ischium, the right femur, and the right fibula. This new specimen is referred to the new species Torvoneustes jurensis sp. nov. as part of the large-bodied macrophagous tribe Geosaurini. Torvoneustes jurensis presents a unique combination of cranial and dental characters including a smooth cranium, a unique frontal shape, acute ziphodont teeth, an enamel ornamentation made of numerous apicobasal ridges shifting to small ridges forming an anastomosed pattern toward the apex of the crown and an enamel ornamentation touching the carina. The description of this new species allows to take a new look at the currently proposed evolutionary trends within the genus Torvoneustes and provides new information on the evolution of this clade.

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

A global reptile assessment highlights shared conservation needs of tetrapods.

Comprehensive assessments of species' extinction risks have documented the extinction crisis1 and underpinned strategies for reducing those risks2. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and 13.6% of birds are threatened with extinction3. Because global assessments have been lacking, reptiles have been omitted from conservation-prioritization analyses that encompass other tetrapods4-7. Reptiles are unusually diverse in arid regions, suggesting that they may have different conservation needs6. Here we provide a comprehensive extinction-risk assessment of reptiles and show that at least 1,829 out of 10,196 species (21.1%) are threatened-confirming a previous extrapolation8 and representing 15.6 billion years of phylogenetic diversity. Reptiles are threatened by the same major factors that threaten other tetrapods-agriculture, logging, urban development and invasive species-although the threat posed by climate change remains uncertain. Reptiles inhabiting forests, where these threats are strongest, are more threatened than those in arid habitats, contrary to our prediction. Birds, mammals and amphibians are unexpectedly good surrogates for the conservation of reptiles, although threatened reptiles with the smallest ranges tend to be isolated from other threatened tetrapods. Although some reptiles-including most species of crocodiles and turtles-require urgent, targeted action to prevent extinctions, efforts to protect other tetrapods, such as habitat preservation and control of trade and invasive species, will probably also benefit many reptiles.

No link between population isolation and speciation rate in squamate reptiles.

Rates of species formation vary widely across the tree of life and contribute to massive disparities in species richness among clades. This variation can emerge from differences in metapopulation-level processes that affect the rates at which lineages diverge, persist, and evolve reproductive barriers and ecological differentiation. For example, populations that evolve reproductive barriers quickly should form new species at faster rates than populations that acquire reproductive barriers more slowly. This expectation implicitly links microevolutionary processes (the evolution of populations) and macroevolutionary patterns (the profound disparity in speciation rate across taxa). Here, leveraging extensive field sampling from the Neotropical Cerrado biome in a biogeographically controlled natural experiment, we test the role of an important microevolutionary process-the propensity for population isolation-as a control on speciation rate in lizards and snakes. By quantifying population genomic structure across a set of codistributed taxa with extensive and phylogenetically independent variation in speciation rate, we show that broad-scale patterns of species formation are decoupled from demographic and genetic processes that promote the formation of population isolates. Population isolation is likely a critical stage of speciation for many taxa, but our results suggest that interspecific variability in the propensity for isolation has little influence on speciation rates. These results suggest that other stages of speciation-including the rate at which reproductive barriers evolve and the extent to which newly formed populations persist-are likely to play a larger role than population isolation in controlling speciation rate variation in squamates.

Compositional features and pattern of codon usage for mitochondrial CO genes among reptiles.

The phenomenon of non-random occurrence of synonymous nucleotide triplets (codons) in the coding sequences of genes is the codon usage bias (CUB). In this study, we used bioinformatic tool kit to analyze the compositional pattern and CUB of mitogenes namely COI, COII and COIII across different orders of reptiles. Estimation of overall base composition in the protein-coding sequences of COI, COII and COIII genes of the reptilian orders revealed an uneven usage of nucleotides. The overall count of A nucleotide was found to be the highest while the overall count of G nucleotide was the least. The CO genes across the three reptilian orders were prominently AT biased. Comparison of the GC proportion at each codon position displayed that GC1 percentage ranked the highest in all the three CO genes of the reptilian orders. SCUO values indicated weaker CUB, while considerable variation of SCUO values existed in the three CO genes across the studied reptiles. Relative synonymous codon usage (RSCU) values indicated that mostly the A ending codons were preferred. Based on the parameters namely neutrality plot, mutational responsive index and translational selection, we could conclude that natural selection was the major evolutionary force in COI, COII and COIII genes in the studied reptilian orders. However, correspondence analysis, parity plot and correlation studies indicated the existence of mutation pressure as well on the CO genes.

Early giant reveals faster evolution of large body size in ichthyosaurs than in cetaceans.

Body sizes of marine amniotes span six orders of magnitude, yet the factors that governed the evolution of this diversity are largely unknown. High primary production of modern oceans is considered a prerequisite for the emergence of cetacean giants, but that condition cannot explain gigantism in Triassic ichthyosaurs. We describe the new giant ichthyosaur Cymbospondylus youngorum sp. nov. with a 2-meter-long skull from the Middle Triassic Fossil Hill Fauna of Nevada, USA, underscoring rapid size evolution despite the absence of many modern primary producers. Surprisingly, the Fossil Hill Fauna rivaled the composition of modern marine mammal faunas in terms of size range, and energy-flux models suggest that Middle Triassic marine food webs were able to support several large-bodied ichthyosaurs at high trophic levels, shortly after ichthyosaur origins.

A Reexamination of the Herpetofauna of Oaxaca, Mexico: Composition Update, Physiographic Distribution, and Conservation Commentary.

A substantial number of changes to the composition of the herpetofauna of the Mexican state of Oaxaca, including taxonomic additions and deletions, have occurred in the five years since our original assessment of this region. These changes now establish a herpetofauna of 480 species for the state. A number of taxonomic and nomenclatural changes involving the Oaxacan herpetofauna also are discussed. Updated patterns of physiographic distribution, endemism, and conservation status of the members of the state herpetofauna are examined.